A phenomenological model with time-varying excitation and inhibition was developed to study possible neural mechanisms underlying changes in the representation of temporal envelopes along the auditory pathway. A modified version of an existing auditory-nerve model [Zhang et al., J. Acoust. Soc. Am. 109, 648–670 (2001)] was used to provide inputs to higher hypothetical processing centers. Model responses were compared directly to published physiological data at three levels: the auditory nerve, ventral cochlear nucleus, and inferior colliculus. Trends and absolute values of both average firing rate and synchrony to the modulation period were accurately predicted at each level for a wide range of stimulus modulation depths and modulation frequencies. The diversity of central physiological responses was accounted for with realistic variations of model parameters. Specifically, enhanced synchrony in the cochlear nucleus and rate-tuning to modulation frequency in the inferior colliculus were predicted by choosing appropriate relative strengths and time courses of excitatory and inhibitory inputs to postsynaptic model cells. The proposed model is fundamentally different than others that have been used to explain the representation of envelopes in the mammalian midbrain, and it provides a computational tool for testing hypothesized relationships between physiology and psychophysics.

1.
Batra
,
R.
(
2004
). “
Responses to amplitude-modulated tones of neurons in the ventral nucleus of the lateral lemniscus of the unanesthetized rabbit
,”
Assoc. Res. Otolaryngol. Abstr.
27
,
914
.
2.
Carney
,
L. H.
(
1993
). “
A model for the responses of low-frequency auditory-nerve fibers in cat
,”
J. Acoust. Soc. Am.
93
,
401
417
.
3.
Carney
,
L. H.
, and
Yin
,
T. C. T.
(
1989
). “
Responses of low-frequency cells in the inferior colliculus to interaural time differences of clicks: Excitatory and inhibitory components
,”
J. Neurophysiol.
62
,
144
161
.
4.
Carney
,
L. H.
,
Heinz
,
M. G.
,
Evilsizer
,
M. E.
,
Gilkey
,
R. H.
, and
Colburn
,
H. S.
(
2002
). “
Auditory phase opponency: A temporal model for masked detection at low frequencies
,”
Acust. Acta Acust.
88
,
334
347
.
5.
Caspary
,
D. M.
,
Palombi
,
P. S.
, and
Hughes
,
L. F.
(
2002
). “
GABAergic inputs shape responses to amplitude modulated stimuli in the inferior colliculus
,”
Hear. Res.
168
,
163
173
.
6.
Caspary
,
D. M.
,
Backoff
,
P. M.
,
Finlayson
,
P. G.
, and
Palombi
,
P. S.
(
1994
). “
Inhibitory inputs modulate discharge rate within frequency receptive fields of anteroventral cochlear nucleus neurons
,”
J. Neurophysiol.
72
,
2124
2132
.
7.
Cooper
,
N. P.
,
Robertson
,
D.
, and
Yates
,
G. K.
(
1993
). “
Cochlear nerve fiber responses to amplitude-modulated stimuli: Variations with spontaneous rate and other response characteristics
,”
J. Neurophysiol.
70
,
370
386
.
8.
Dau
,
T.
,
Kollmeier
,
B.
, and
Kohlrausch
,
A.
(
1997
). “
Modeling auditory processing of amplitude modulation. I. Modulation detection and masking with narrow-band carriers
,”
J. Acoust. Soc. Am.
102
,
2892
2905
.
9.
Elhilali
,
M.
,
Fritz
,
J. B.
,
Klein
,
D. J.
,
Simon
,
J. Z.
, and
Shamma
,
S. A.
(
2004
). “
Dynamics of precise spike timing in primary auditory cortex
,”
J. Neurosci.
24
,
1159
1172
.
10.
Ewert
,
S. D.
,
Verhey
,
J. L.
, and
Dau
,
T.
(
2002
). “
Spectro-temporal processing in the envelope-frequency domain
,”
J. Acoust. Soc. Am.
112
,
2921
2931
.
11.
Faure
,
P. A.
,
Fremouw
,
T.
,
Casseday
,
J. H.
, and
Covey
,
E.
(
2003
). “
Temporal masking reveals properties of sound-evoked inhibition in duration-tuned neurons of the inferior colliculus
,”
J. Neurosci.
24
,
3052
3065
.
12.
Frisina
,
R. D.
,
Smith
,
R. L.
, and
Chamberlain
,
S. C.
(
1990
). “
Encoding of amplitude modulation in the gerbil cochlear nucleus. I. A hierarchy of enhancement
,”
Hear. Res.
44
,
99
122
.
13.
Goldberg
,
J. M.
, and
Brown
,
P. B.
(
1969
). “
Responses of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: Some physiological mechanisms of sound localization
,”
J. Neurophysiol.
22
,
613
636
.
14.
Grothe
,
B.
(
1994
). “
Interaction of excitation and inhibition in processing of pure tone and amplitude-modulated stimuli in the medial superior olive of the mustached bat
,”
J. Neurophysiol.
71
,
706
721
.
15.
Harris
,
D. M.
, and
Dallos
,
P.
(
1979
). “
Forward masking of auditory nerve fiber responses
,”
J. Neurophysiol.
42
,
1083
1107
.
16.
Heinz
,
M. G.
,
Colburn
,
H. S.
, and
Carney
,
L. H.
(
2001a
). “
Rate and timing cues associated with the cochlear amplifier: Level discrimination based on monaural cross-frequency coincidence detection
,”
J. Acoust. Soc. Am.
110
,
2065
2084
.
17.
Heinz
,
M. G.
,
Zhang
,
X.
,
Bruce
,
I. C.
, and
Carney
,
L. H.
(
2001b
). “
Auditory-nerve model for predicting performance limits of normal and impaired listeners
,”
JARO
2
,
91
96
.
18.
Hewitt
,
M. J.
, and
Meddis
,
R.
(
1994
). “
A computer model of amplitude-modulation sensitivity of single units in the inferior colliculus
,”
J. Acoust. Soc. Am.
95
,
2145
2159
.
19.
Joris
,
P. X.
, and
Yin
,
T. C. T.
(
1992
). “
Responses to amplitude-modulated tones in the auditory nerve of the cat
,”
J. Acoust. Soc. Am.
91
,
215
232
.
20.
Joris
,
P. X.
, and
Yin
,
T. C. T.
(
1998
). “
Envelope coding in the lateral superior olive. III. Comparison with afferent pathways
,”
J. Neurophysiol.
79
,
253
269
.
21.
Krishna
,
B. S.
, and
Semple
,
M. N.
(
2000
). “
Auditory temporal processing: Responses to sinusoidally amplitude-modulated tones in the inferior colliculus
,”
J. Neurophysiol.
84
,
255
273
.
22.
Krukowski
,
A. E.
, and
Miller
,
K. D.
(
2001
). “
Thalamocortical NMDA conductances and intracortical inhibition can explain cortical temporal tuning
,”
Nat. Neurosci.
4
,
424
430
.
23.
Langner
,
G.
(
1981
). “
Neuronal mechanisms for pitch analysis in the time domain
,”
Exp. Brain Res.
44
,
450
454
.
24.
Langner
,
G.
, and
Schreiner
,
C. E.
(
1988
). “
Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms
,”
J. Neurophysiol.
60
,
1799
1822
.
25.
Liberman
,
M. C.
(
1978
). “
Auditory-nerve responses from cats raised in a low-noise chamber
,”
J. Acoust. Soc. Am.
63
,
442
455
.
26.
Miller
,
R. L.
,
Schilling
,
J. R.
,
Franck
,
K. R.
, and
Young
,
E. D.
(
1997
). “
Effects of acoustic trauma on the representation of the vowel /ε/ in cat auditory nerve fibers
,”
J. Acoust. Soc. Am.
101
,
3602
3616
.
27.
Oertel
,
D.
(
1983
). “
Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus
,”
J. Neurosci.
3
,
2043
2053
.
28.
Oliver, D. L., and Huerta, M. F. (1992). “Inferior and superior colliculi,” in The Mammalian Auditory Pathway: Neuroanatomy, edited by D. R. Webster, A. N. Popper, and R. R. Fay (Springer Verlag, New York), pp. 168–221.
29.
Oxenham
,
A. J.
, and
Shera
,
C. A.
(
2003
). “
Estimates of human cochlear tuning at low levels using forward and simultaneous masking
,”
JARO
4
,
541
554
.
30.
Palombi
,
P. S.
, and
Caspary
,
D. M.
(
1996
). “
GABA inputs control discharge rate primarily within frequency receptive fields of inferior colliculus neurons
,”
J. Neurophysiol.
75
,
2211
2219
.
31.
Plack
,
C. J.
, and
Oxenham
,
A. J.
(
1998
). “
Basilar-membrane nonlinearity and the growth of forward masking
,”
J. Acoust. Soc. Am.
103
,
1598
1608
.
32.
Rhode
,
W. S.
, and
Greenberg
,
S.
(
1994
). “
Encoding of amplitude modulation in the cochlear nucleus of the cat
,”
J. Neurophysiol.
71
,
1797
1825
.
33.
Ryugo
,
D. K.
, and
Parks
,
T. N.
(
2003
). “
Primary innervation of the avian and mammalian cochlear nucleus
,”
Brain Res. Bull.
60
,
435
456
.
34.
Schneiderman
,
A.
,
Oliver
,
D. L.
, and
Henkel
,
C. K.
(
1988
). “
Connections of the dorsal nucleus of the lateral lemniscus: an inhibitory parallel pathway in the ascending auditory system?
J. Comp. Neurol.
276
,
188
208
.
35.
Schofield
,
B. R.
, and
Cant
,
N. B.
(
1996
). “
Projections from the ventral cochlear nucleus to the inferior colliculus and the contralateral cochlear nucleus in guinea pigs
,”
Hear. Res.
102
,
1
14
.
36.
Shera
,
C. A.
,
Guinan
, Jr.,
J. J.
, and
Oxenham
,
A. J.
(
2002
). “
Revised estimates of human cochlear tuning from otoacoustic and behavioral measurements
,”
Proc. Natl. Acad. Sci. U.S.A.
99
,
3318
3323
.
37.
Sinex
,
D. G.
,
Sabes
,
J. H.
, and
Li
,
H.
(
2002
). “
Responses of inferior colliculus neurons to harmonic and mistuned complex tones
,”
Hear. Res.
168
,
150
162
.
38.
Smith
,
R. L.
(
1977
). “
Short-term adaptation in single auditory nerve fibers: Some post-stimulatory effects
,”
J. Neurophysiol.
40
,
1098
1111
.
39.
Smith
,
R. L.
, and
Brachman
,
M. L.
(
1980
). “
Response modulation of auditory-nerve fibers by AM stimuli: Effects of average intensity
,”
Hear. Res.
2
,
123
133
.
40.
Smith
,
R. L.
, and
Zwislocki
,
J. J.
(
1975
). “
Short-term adaptation and incremental responses of single auditory-nerve fibers
,”
Biol. Cybern.
17
,
169
182
.
41.
Svirskis
,
G.
, and
Rinzel
,
J.
(
2003
). “
Influence of subthreshold nonlinearities on signal-to-noise ratio and timing precision for small signals in neurons: Minimal model analysis
,”
Network Comput. Neural Syst.
14
,
137
150
.
42.
Viemeister
,
N. F.
(
1979
). “
Temporal modulation transfer functions based upon modulation thresholds
,”
J. Acoust. Soc. Am.
66
,
1364
1380
.
43.
Westerman
,
L. A.
, and
Smith
,
R. L.
(
1988
). “
A diffusion model of the transient response of the cochlear inner hair cell synapse
,”
J. Acoust. Soc. Am.
83
,
2266
2276
.
44.
Wickesberg
,
R. E.
, and
Oertel
,
D.
(
1988
). “
Tonotopic projection from the dorsal to the anteroventral cochlear nucleus of mice
,”
J. Comp. Neurol.
268
,
389
399
.
45.
Wu
,
S. H.
,
Ma
,
C. L.
,
Sivaramakrishnan
,
S.
, and
Oliver
,
D. L.
(
2002
). “
Synaptic modification in neurons of the central nucleus of the inferior colliculus
,”
Hear. Res.
168
,
43
54
.
46.
Yin, T. C. T. (2002). “Neural mechanisms of encoding binaural localization cues in the auditory brainstem,” in Integrative Functions in the Mammalian Auditory Pathway, edited by D. Oertel, A. N. Popper, and R. R. Fay (Springer Verlag, New York), pp. 99–159.
47.
Zhang, X. (2004). Personal communication.
48.
Zhang
,
X.
,
Heinz
,
M. G.
,
Bruce
,
I. C.
, and
Carney
,
L. H.
(
2001
). “
A phenomenological model for the responses of auditory-nerve fibers: I. Non-linear tuning with compression and suppression
,”
J. Acoust. Soc. Am.
109
,
648
670
.
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